Deciphering the Heteropterys pannosa species complex (Malpighiaceae)

We describe three new species of Malpighiaceae that are endemic to central Brazil and related to the Heteropterys pannosa complex, a group of xylopodiferous, unbranched subshrubs with fruit in mericarps that have a strongly reduced or no dorsal wing. Heteropterys tocantinensis is more common in eastern Tocantins State and on the border with Bahia State, and there are a few records from Mato Grosso State. Heteropterys veadeirensis is restricted to northern Goiás State and H. walteri has a wider distribution, occurring in some municipalities in northern Goiás and southern Tocantins. Additionally, we also provide detailed redescriptions of H. pannosa and H. rosmarinifolia, the two previously known species in this complex. All species are considered Endangered (EN) based on IUCN criteria, especially due to the low area of occupancy. Illustrations, distribution maps, and information about phenology and habitat are also provided for all taxa.


INTRODUCTION
Heteropterys Kunth is a highly diverse genus of Malpighiaceae due to its remarkable vegetative and reproductive morphological variability. It comprises approximately 158 species that are distributed from Mexico to South America, including the West Indies (Anderson, 2001a;Anderson, 2013;Amorim & Marinho, 2020). Only Heteropterys leona (Cav.) Exell has a disjunct intercontinental distribution. It occurs from Belize to northern Brazil and on the west coast of Africa (Anderson, 2001a). The species of Heteropterys are subshrubs, shrubs, small trees or robust lianas and has a single synapomorphy: the fruit is a schizocarp where each mericarp or nut has a dominant dorsal wing with a thick inferior margin and lateral wings that are absent or rarely strongly reduced (Amorim, 2003;Pessoa & Amorim, 2016). The genus was recovered as monophyletic and well-placed in the tetrapteroid lineage, which basically comprises plants with a mericarp with dominant lateral wings and a reduced or no dorsal wing (Davis & Anderson, 2010).
Despite the extensive research conducted to solve the problematic taxonomy of Heteropterys, in the last 10 years, novelties in this genus have been constantly reported from different habitats. These novelties can often be placed in informal groups supported by lineages in a recent Heteropterys phylogeny (C.C. Davis & A.M. Amorim, 2021, personal communication), which sometimes correspond to infrageneric categories, such as those proposed by Niedenzu (1903Niedenzu ( , 1928. Notable examples are new taxa of Heteropterys recently revealed in the Aptychia (Amorim & Marinho, 2020), Metallophyllis (Amorim et al., 2017), Parabanisteria (Almeida & Pellegrini, 2021), Rhodopetalis (Pessoa & Amorim, 2016), Stenophyllarion (Sebastiani & Mamede, 2010) and Xanthopetalis groups (Anderson, 2014;Pessoa, Marinho & Amorim, 2019). Likewise, the resolution of Malpighiaceae species complexes in different genera have been constantly investigated with the objective of clarifying the vegetative and reproductive variability among close species. For example, the resolution of the Amorimia rigida complex (Almeida, Berg & Amorim, 2016) where three new species were proposed, the Galphimia langlassei complex (Anderson, 2003) where two new species were proposed, and the Mascagnia cordifolia complex (Anderson, 2005) and Mascagnia sepium complex (Anderson, 2001b) where three and seven new species were proposed, respectively. In Heteropterys we can highlight the resolution of Heteropterys anomala complex (Amorim, 2003), where four new species were proposed and Heteropterys oblongifolia complex (Anderson, 1981) where one new species was proposed but is argued that other taxonomic novelties might arise when a larger number of collections is available to the complex.
The Parabanisteria group is the most diversified lineage of Heteropterys. It comprises at least 44 species and occurs in several habitats, such as upland forests, white-sand vegetation and floodplains forests in the Amazon basin. It is also occasionally found in tabuleiro and mussununga forests (i.e., two kinds of white-sand forest in northeastern Brazil) and a few species occur in inselberg vegetation in the Atlantic Forest domain. However, most species of the Parabanisteria group occur in central Brazil and grow in clay or sand in highland savannas, gallery forests, dry forests and on rock outcrops in the Cerrado domain. Species of this group are recognized by their inflorescence rachis, peduncle, pedicels and sepals covered by a ferrugineous indumentum, eglandular bracteoles at the apex of the peduncle, sepals concealing the petals in bud and revolute at anthesis, and petals spreading and all vivid yellow (Anderson, 1981;Anderson, 2001a). The mericarp is strongly variable in form and size but generally has a large dorsal wing and lacks lateral wings or crests.
Many species in the Parabanisteria group have morphological characteristics adapted to open vegetation in the Cerrado domain, such as an arborescent or shrubby habit with woody stems, coriaceous leaves and inflorescences that often develop after deciduous leaves period. Among them, Heteropterys pannosa Griseb. stands out. It is a subshrub with a xylopodiferous underground stem system, erect and elongate pseudoraceme inflorescences and mericarps without a dorsal wing or with this structure strongly reduced to an apical crest (Figs.1A,1K and 2A,2B). Heteropterys pannosa was described from a collection made by Johann Emanuel Pohl in Goiás State (Grisebach, 1858). Since then, that name has been applied to many collections from different localities at central Brazil (Fig. 3A). Our study clarified the geographical and morphological patterns along the distribution of the H. pannosa species complex and that this complex comprises more than just the two species currently recognized: H. pannosa and the recently described H. rosmarinifolia R.F.Almeida & M.Pell. Thus, in this work we describe three new species We also include an identification key, distribution maps, illustrations, and the estimated conservation status for all the species related in the H. pannosa complex.

MATERIALS AND METHODS
We analyzed 82 specimens of the Heteropterys pannosa complex from the ALCB, CEPEC, CEN, ESA, HUEFS, MBM, MICH, NY, RB, UB, UESC, UFG, SP and SPF herbaria (acronyms following Thiers, 2021-continuously updated). We also used web-based resources, such as the Reflora Virtual Herbarium (Available at http://reflora.jbrj.gov.br and accessed in November 2021) and SpeciesLink (Available at https://specieslink.net/ and accessed in November 2021), to check additional specimens (as digital images), including types. Herbaria consulted by digital images are indicated by an asterisk in specimens examined. Descriptions of the characters are based on dried material. The geographic distributions maps were created using the website SimpleMappr (Shorthouse, 2010), with subsequent style modifications. The conservation status of each species was assessed using IUCN Standards & Petitions Subcommittee (2017) guidelines and criteria; the area of occupancy and extent of occurrence were calculated using GeoCAT (Bachman et al., 2011). The electronic version of this article in Portable Document Format (PDF) will represent a published work according to the International Code of Nomenclature for algae, fungi, and plants (ICN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. In addition, new names contained in this work which have been issued with identifiers by IPNI will eventually be made available to the Global Names Index. The IPNI LSIDs can be resolved and the associated information viewed through any standard web browser by appending the LSID contained in this publication to the prefix "http://ipni.org/". The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central SCIE, and CLOCKSS.

RESULTS
Key to the species of the Heteropterys pannosa complex Description Subshrub, 0.2-0.8 m tall, stems erect, cylindrical, 1-2(-3) mm diam., sericeous to glabrate with age, lenticels not seen, unbranched or nearly so, all arising from a xylopodium. Leaves opposite or occasionally 3-whorled on the same stem, internodes 2-4(-6.8) cm long; petiole (1.5-)3-5 mm long, densely sericeous to glabrate with age, eglandular; stipules not seen; lamina of larger leaves 5.7-9(-11.7) cm long, (0.7-)1.1-3 cm wide, densely sericeous or tomentose-ferrugineous to irregularly glabrate with age on basal leaves and densely and persistently sericeous or tomentose-ferrugineous on leaves closer to the inflorescence, subcoriaceous to coriaceous, not conduplicate, elliptical, lanceolate or oblong to slightly obovate, the base cuneate, rarely obtuse or attenuate, the apex obtuse or sometimes (on the same stem) gradually tapered and becoming acute or acuminate, the margins entire or rarely slightly revolute, glands in abaxial surface absent or inconspicuous, hidden by indumentum, the lateral veins and reticulum prominent, especially on the abaxial surface.

Distribution, phenology and conservation status
Heteropterys pannosa occurs in Goiás State and for the first time is recorded for Minas Gerais State (Fig. 3B). It grows in sandy soils (i.e., quartzite and plinthite formation, Fig. 2A

Remarks
The type collection of Heteropterys pannosa, gathered by Johann Emanuel Pohl (1782Pohl ( -1834 in Goiás State, does not have a date and is annotated with the enigmatic locality of "Serra S. Felis bei Rio Custódio." Based on the travel diary of Johann Emanuel Pohl that narrates the details of his journey in Brazil (Pohl, 1976), we assume that the type was collected on 8 July 1819, the only time Pohl was in this locality. In this diary, Pohl also notes that the Custódio River is near the Traíras and Maranhão rivers (Pohl, 1976).
An antique map of Goiás State (ArPDF, 2020) shows "Chapada de São Félix" (i.e., annotated by Pohl as "Serra de S. Felis"). This plateau is near the Maranhão River, which is actually denominated the Tocantins River. The point on the map for Goiás State (ArPDF, 2020) is at 13 latitude. We carefully looked at this region using Google MapsÒ and found the Custódio River, which is part of the Tocantins River hydrographic basin. Thus, this region is probably the H. pannosa type collection locality and is delimited by the municipalities of Minaçu in Goiás State and Paranã in Tocantins State. The vegetative morphology of Heteropterys pannosa is extremally variable (Figs. 1A-1D). In the type (Pohl 1940) and several other collections (e.g., Souza 24795, Fig. 1B), the shape of the leaf lamina is elliptic. In other collections, the lamina is lanceolate (e.g., Queiroz 15056, Fig. 1D) or oblong-obovate (e.g., Hatschbach 54683, Figs. 1A, 1D). Further, many collections have different lamina shapes on the same stem (e.g., especially Anderson 6673) and a large variation in the indumentum density caused by the gradual loss of trichomes. For these reasons, the absence of diagnostic differences in reproductive characteristics and the fact that many individuals occur in sympatry in some areas (C. Anderson, 2003, pers. comm.), we decided to define H. pannosa within a broad concept. This position should be re-evaluated when extensive fieldwork can be conducted throughout the area of occurrence and there are more and better specimens are available for study. The vegetative and reproductive characters of H. pannosa are illustrated for the first time. Description Subshrub, 0.2-0.8(-1.2) m tall, stems erect, cylindrical, 1.5-2 mm diam., densely sericeous to glabrate with age, developing scattered lenticels, unbranched or nearly so, all arising from a xylopodium. Leaves opposite or usually 3-4-whorled on the same stem, internodes 0.3-2(-2.5) cm; petiole 1-3 mm long, sericeous to glabrate, eglandular; stipules ca. 0.5 mm long, persistent, generally hidden by indumentum; lamina of larger leaves 1.3-11.4 cm long, 0.1-1.3 cm wide, abaxial surface very sparsely sericeous to glabrate with age or densely and persistently sericeous on leaves near the inflorescence, adaxial surface glabrate, subcoriaceous to coriaceous, strongly conduplicate, linear or narrowly oblongoblanceolate, the base acute, the apex acuminate or rarely acute, the margins entire to slightly revolute, abaxial surface sometimes with two large glands at base and usually a row of smaller impressed and inconspicuous glands near or somewhat inside the margin, glands rarely absent, the lateral veins and reticulum prominent on both surfaces. Inflorescence a pseudoraceme, axillary or terminal, erect, (1-)3.5-10.5 cm long, densely sericeous-ferrugineous, with irregular internodes between each pair of flowers, mostly comprising (4-)10-16 flowers distributed throughout the rachis; bracts 2-4 mm long, 0.7-1 mm wide, sparsely sericeous, linear-lanceolate, margins entire, eglandular or with 1-2 glands at base, the glands ca. 0.2 mm diam., persistent; peduncle 6-10 mm long, sericeous-ferrugineous; bracteoles apical, 1-2.8 mm long, 0.5-1 mm wide, sparsely sericeous, lanceolate, persistent, eglandular or with 1-2 glands at base, the glands ca. 0.2 mm diam.; pedicel 5-9(-11.5) mm long, 0.5-1.1 mm wide, uniformly slender, sericeous-ferrugineous. Sepals 4-5.5 mm long, 1.5-2.3 mm wide, narrowly ovate, acute at apex, revolute at anthesis, not appressed against filaments at anthesis, abaxially sericeous-ferrugineous, adaxially green and glabrous, all eglandular or all biglandular or the anterior sepal eglandular and the four lateral sepals biglandular, the glands 1-2 mm diam., green. Petals not exposed in the enlarging bud, vivid yellow, glabrous, membranaceous, not keeled, irregularly erose and eglandular at the margin, the posterior-lateral and anterior-lateral petals similar to each other, spreading, the claw 1-3.7 mm long, the limb 3.5-6 mm long, 2.5-5.5 mm wide; posterior petal spreading, the claw 1-2.5 mm long, the limb 3.4-5.3 mm long, 2.4-4 mm wide. Stamens with filaments slightly heteromorphic, longer opposite sepals than opposite petals, glabrous, 2.5-4.5 mm long, 0.9-1 mm wide, all straight and slender, basally connate; anthers 1-1.2 mm long, glabrous, irregularly reflexed at anthesis, all alike; the connective uniformly yellow. Ovary 1.1-1.5 mm tall, sericeous-ferrugineous; styles 3-3.5 mm long, slightly unequal, larger than the largest stamens, the anterior style erect and straight, the two posterior styles slightly divergent, glabrous, obtuse at apex; stigmas lateral, all three facing the center of the flower. Fruit unknown.

Distribution, phenology and conservation status
The recently described Heteropterys rosmarinifolia was originally known from two specimens collected in the Serra do Tombador Natural Reserve (Almeida & Pellegrini, 2021) and was therefore assessed as data deficient (DD) by the authors. We increased the distribution area of the species to another protected area, Chapada dos Veadeiros National Park, which is also in northern Goiás State (Fig. 3C). An extent of occurrence less than 3.000 km 2 and an area of occupancy less than 16 km 2 means H. rosmarinifolia is Endangered (EN) based on IUCN Standards & Petitions Subcommittee (2017) criteria, even though it occurs in two environmental protection areas [B1 + B2a]. Heteropterys rosmarinifolia grows in sandy savannas (Fig. 2C), between 1.100 and 1.300 m a.s.l. This species has been collected with buds and/or flowers from July to September.

Diagnosis
Heteropterys tocantinensis differs from the other species in the H. pannosa complex in its peduncle, which is shorter than the pedicel at anthesis (vs peduncle generally equaling the pedicel or rarely longer), anthers irregularly pilose (vs glabrous), styles dorsally apiculate (vs hooked, obtuse or truncate) and dorsal wing of mericarp present and 5-6 mm wide (vs absent or rarely reduced to an apical crest and 1-3 mm wide).
Distribution, phenology and conservation status Heteropterys tocantinensis occurs in the state of Tocantins, on the border of the states of Bahia and Maranhão. A few records from the state of Mato Grosso were also found, on the border of Goiás State (Fig. 3D). In these locations it grows from 400 and 700 m a.s.l.
Heteropterys tocantinensis is associated with clay soil (Fig. 6A), which is similar to the habitat of H. walteri and differs from H. pannosa, H. rosmarinifolia, and H. veadeirensis, which are associated with sandy soils. The species has been collected with buds and/or flowers in March and from September to January and with fruits from September to November. Although H. tocantinensis has a broad extant of occurrence, for now it should be considered Endangered (EN) [B2ii], because of its area of occupancy is less than 40 km 2 . New expeditions in areas with clay soil in bordering states might reveal additional populations of H. tocantinensis.

Etymology
The specific epithet refers to the occurrence of the new species near the Tocantins River basin in central Brazil.

Remarks
For some vegetative characters, such as shape, consistency and size of the lamina, Heteropterys tocantinensis resembles H. pannosa and H. walteri. Heteropterys tocantinensis can be differentiated by the stems and leaves covered by a sericeous indumentum, which is early caducuous (vs stems and leaves glabrous in H. veadeirensis and densely and persistently hispid in H. walteri). Also, in H. tocantinensis the peduncle is strongly reduced, the anthers are pilose and the mericarp has a small dorsal wing, characteristics not observed in other species of this complex. Most records of H. tocantinensis are from Tocantins State but this species is not sympatric with H. walteri, which has an occurrence further south of that state (see Figs. 3D, 3F). Herbarium collections of H. tocantinensis were often misidentified as H. byrsonimifolia A. Juss., a very common species, which generally grows in highland savannas and on rock outcrops but has an arborescent habit and paniculate inflorescence.

Diagnosis
Heteropterys veadeirensis differs from the other species in the H. pannosa complex in its glabrous stems, petiole and lamina (vs densely hispid or sericeous to sparsely sericeous), very sparsely sericeous to glabrate peduncle and pedicel (vs densely hispid, sericeous or tomentose), and styles dorsally short-hooked at the apex (vs obtuse, truncate or slightly apiculate, except in H. walteri).

Distribution, phenology and conservation status
Heteropterys veadeirensis is restricted to northern Goiás State (Fig. 3E) and grows on rock outcrops (Fig. 6C) between 1.000 and 1.200 m a.s.l. This species has been collected with buds and/or flowers from July to November and with fruits from August to October. Almost all records were recorded from a protected area called Chapada dos Veadeiros National Park; the only exception is a collection made about 300 km to the south, in the municipality of Cristalina. Although these populations are protected and there is a considerable distance between the two localities, the species is assessed as Endangered (EN) according to IUCN Standards & Petitions Subcommittee (2017) criteria. The extent of occurrence is less than 4,000 km 2 and area of occupancy less than 28 km 2 . We still do not know if the specimens from Alto Paraíso de Goiás belong to only one population, but it is likely that there are fewer than five populations [B1 + B2a].  Description Subshrub, 0.3-0.5 m tall, stems erect, cylindrical, ca. 4 mm diam., densely hispid to glabrate with age, lenticels not seen, unbranched or nearly so, all arising from a xylopodium. Leaves opposite or rarely 3-whorled on the same stem; petiole 3-5 mm long, densely hispid, eglandular; stipules minute, ca. 0.5 mm long, hidden by indumentum; lamina of larger leaves (6.7-)8-11.8(-14) cm long, 3.2-7.2 cm wide, abaxially and adaxially densely tomentose, glabrescent with age, the midrib and primary veins on both surfaces densely hispid, coriaceous, oblong or slightly obovate, rarely elliptical, the base cuneate or rarely obtuse, the apex rounded and often mucronate, the margins entire, sometimes with two large glands abaxially at base and usually with 7-13 smaller impressed glands in an inframarginal row on each side of the lamina or rarely glands absent, the glands ca. 0.5 mm diam., the lateral veins and reticulum prominent on abaxial surface. Inflorescence a pseudoraceme, mostly elongate, axillary or terminal, erect, 8-16(-19.5) cm long, densely hispid, with measurable and irregular internodes between each groups of 2-3 flowers, mostly comprising 14-21 flowers distributed throughout the rachis; bracts 2-3 mm long, ca. 1 mm wide, abaxially densely hispid to tomentose, linear-lanceolate, persistent, margins entire, eglandular or with 1-2 glands near the base, the glands ca. 0.5 mm diam., generally hidden by indumentum; peduncle 5-8 mm long, ca. 1 mm wide, densely hispid; bracteoles apical, 1.7-2 mm long, ca. 0.5 mm wide, abaxially densely hispid to tomentose, linearlanceolate, persistent, eglandular or with 1-2 glands near the base, the glands ca. 0.3 mm diam., hidden by indumentum; pedicel 5.5-7 mm long, ca. 1 mm wide, uniformly slender, densely hispid. Sepals 3.5-4 mm long, 1.5-2 mm wide, narrowly ovate, acute at apex, revolute at anthesis, not appressed against filaments at anthesis, abaxially densely tomentose, adaxially glabrous, the anterior sepal eglandular, the four lateral sepals biglandular, the glands 1-1.5 mm diam. Petals not exposed in the enlarging bud, vivid yellow, glabrous, membranaceous, not keeled, erose and eglandular at the margin, the posterior-lateral and anterior-lateral petals similar to each other, spreading, the claw 3-4 mm long, the limb 3.5-4.5 mm long, 3.5-4.5 mm wide; posterior petal spreading, the claw 3.5-4 mm long, the limb 5-5.3 mm long, 4-4.4 mm wide. Stamens with filaments heteromorphic, longer opposite sepals than opposite petals, glabrous, 2.5-3 mm long, 0.3-0.5 mm wide, all straight and slender, basally connate; anthers 0.8-1 mm long, glabrous, slightly reflexed at anthesis, all alike; the connective proximally dark brown, distally yellow. Ovary 1.3-1.5 mm tall, densely sericeous-ferrugineous; styles 1.7-2 mm long, slightly unequal, equaling or slightly exceeding the anthers, the anterior style erect and straight, the two posterior styles divergent, glabrous, dorsally short-hooked at apex; stigmas lateral, all three facing the center of the flower. Mericarp with rounded nut, 9-12 mm long, 7-10 mm wide, with several parallel longitudinal veins on each side, densely sericeous-ferrugineous, the trichomes persistent; lateral wings or crests absent; dorsal wing absent or strongly reduced to an apical crest, a crest arising slightly at the style, 1-3 mm wide, widest near distal side of nut; ventral areole 3-5 mm tall, 3-5 mm wide, ovate.